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Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities

Predicting evolution in microbial communities is critical for problems from human health to global nutrient cycling. Understanding how species interactions impact the distribution of fitness effects for a focal population would enhance our ability to predict evolution. Specifically, does the type of...

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Autores principales: Martinson, Jonathan N. V., Chacón, Jeremy M., Smith, Brian A., Villarreal, Alex R., Hunter, Ryan C., Harcombe, William R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689784/
https://www.ncbi.nlm.nih.gov/pubmed/37865718
http://dx.doi.org/10.1038/s41396-023-01534-6
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author Martinson, Jonathan N. V.
Chacón, Jeremy M.
Smith, Brian A.
Villarreal, Alex R.
Hunter, Ryan C.
Harcombe, William R.
author_facet Martinson, Jonathan N. V.
Chacón, Jeremy M.
Smith, Brian A.
Villarreal, Alex R.
Hunter, Ryan C.
Harcombe, William R.
author_sort Martinson, Jonathan N. V.
collection PubMed
description Predicting evolution in microbial communities is critical for problems from human health to global nutrient cycling. Understanding how species interactions impact the distribution of fitness effects for a focal population would enhance our ability to predict evolution. Specifically, does the type of ecological interaction, such as mutualism or competition, change the average effect of a mutation (i.e., the mean of the distribution of fitness effects)? Furthermore, how often does increasing community complexity alter the impact of species interactions on mutant fitness? To address these questions, we created a transposon mutant library in Salmonella enterica and measured the fitness of loss of function mutations in 3,550 genes when grown alone versus competitive co-culture or mutualistic co-culture with Escherichia coli and Methylorubrum extorquens. We found that mutualism reduces the average impact of mutations, while competition had no effect. Additionally, mutant fitness in the 3-species communities can be predicted by averaging the fitness in each 2-species community. Finally, we discovered that in the mutualism S. enterica obtained vitamins and more amino acids than previously known. Our results suggest that species interactions can predictably impact fitness effect distributions, in turn suggesting that evolution may ultimately be predictable in multi-species communities.
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spelling pubmed-106897842023-12-02 Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities Martinson, Jonathan N. V. Chacón, Jeremy M. Smith, Brian A. Villarreal, Alex R. Hunter, Ryan C. Harcombe, William R. ISME J Article Predicting evolution in microbial communities is critical for problems from human health to global nutrient cycling. Understanding how species interactions impact the distribution of fitness effects for a focal population would enhance our ability to predict evolution. Specifically, does the type of ecological interaction, such as mutualism or competition, change the average effect of a mutation (i.e., the mean of the distribution of fitness effects)? Furthermore, how often does increasing community complexity alter the impact of species interactions on mutant fitness? To address these questions, we created a transposon mutant library in Salmonella enterica and measured the fitness of loss of function mutations in 3,550 genes when grown alone versus competitive co-culture or mutualistic co-culture with Escherichia coli and Methylorubrum extorquens. We found that mutualism reduces the average impact of mutations, while competition had no effect. Additionally, mutant fitness in the 3-species communities can be predicted by averaging the fitness in each 2-species community. Finally, we discovered that in the mutualism S. enterica obtained vitamins and more amino acids than previously known. Our results suggest that species interactions can predictably impact fitness effect distributions, in turn suggesting that evolution may ultimately be predictable in multi-species communities. Nature Publishing Group UK 2023-10-21 2023-12 /pmc/articles/PMC10689784/ /pubmed/37865718 http://dx.doi.org/10.1038/s41396-023-01534-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Martinson, Jonathan N. V.
Chacón, Jeremy M.
Smith, Brian A.
Villarreal, Alex R.
Hunter, Ryan C.
Harcombe, William R.
Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title_full Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title_fullStr Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title_full_unstemmed Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title_short Mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
title_sort mutualism reduces the severity of gene disruptions in predictable ways across microbial communities
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10689784/
https://www.ncbi.nlm.nih.gov/pubmed/37865718
http://dx.doi.org/10.1038/s41396-023-01534-6
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